BioRisk | of 263-269 (2022) Apeer-reviewed open-access journal

doi: 10.3897/biorisk.17.75988 RESEARCH ARTICLE & B Ke) RP IS k

https://biorisk.pensoft.net

Sexually-manifested variations in pigmentation
of Boeckella poppei (Copepoda, Calanoida) from
Livingston Island (Maritime Antarctica)

Ivan Pandourski', Vesela Evtimova', Lyubomir Kenderov*

| Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Science, Sofia 1000, Bulgaria
2 Faculty of Biology, Sofia University “St. Kliment Ohridski’, Sofia 1164, Bulgaria

Corresponding author: Vesela Evtimova (vesela.evtimova@gmail.com)

Academic editor: Vlada Peneva | Received 22 October 2021 | Accepted 21 December 2021 | Published 21 April 2022

Citation: Pandourski I, Evtimova V, Kenderov L (2022) Sexually-manifested variations in pigmentation of
Boeckella poppei (Copepoda, Calanoida) from Livingston Island (Maritime Antarctica). In: Chankova S, Peneva V,
Metcheva R, Beltcheva M, Vassilev K, Radeva G, Danova K (Eds) Current trends of ecology. BioRisk 17: 263-269.
https://doi.org/10.3897/biorisk.17.75988

Abstract

Antarctic environments are exposed to high levels of ultraviolet radiation (UVR) that are often detrimen-
tal to their biota. Recent studies suggest that the genus Boeckella (Copepoda, Calanoida) has a high level
of plasticity in terms of its reaction to UVR, which enables its wide distribution in various water bodies
in Antarctica. Boeckella poppei is common in freshwater habitats of all three main biogeographic regions
in Antarctica: sub-Antarctic islands, maritime and continental. We present for the first time a specific
photoprotective response in populations of B. poppei from Livingston Island, Maritime Antarctica. In
non-ovigerous females and in males, we observed uniform distribution of carotenoids in the body, while
these pigments were almost entirely concentrated in the ovisacs of mature females. We consider this as a
means of progeny protection from the teratogenic influence of the high level of UVR in Antarctic envi-
ronments. Unequivocally, such adaptation would facilitate the expansion of B. poppei on the continent
through colonisation and survival in shallow freshwater habitats. Given that the Antarctic environment is
dynamically changing over the past decades and the accelerated retreat of permanent ice cover is a prem-
ise for the formation of shallow ponds, B. poppei could be a suitable indicator for reflecting the ongoing
global environmental changes in Antarctica.

Keywords

Bulgarian Antarctic Base, copepod pigmentation, freshwater, ovigerous females, progeny photoprotection

Copyright Ivan Pandourski et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC
BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

264 Ivan Pandourski et al. / BioRisk 17: 263-269 (2022)

Introduction

Solar radiation is an essential modulator of the functioning of natural ecosystems (Wet-
zel 2003). Ambient levels of biologically-damaging ultraviolet radiation (UVR) have
been rising in aquatic systems in Polar Regions (Karentz and Bosch 2001; Perin and
Lean 2004). During the 20" century, the release of anthropogenic contaminants in-
creased the potential for photoactivated toxicity in these aquatic systems, triggering the
organisms to develop mechanisms to minimise phototoxic damage (Diamond 2003).

The calanoid copepod Boeckella poppei (Mrazek, 1901) is widely distributed in
freshwater habitats in the three main biogeographic regions in Antarctica: sub-Antarc-
tic islands, maritime and continental Antarctica (Maturana et al. 2019). On Living-
ston Island, the species has been reported from the Hurd Peninsula (Pandourski and
Apostolov 2004) and in most of the 15 studied lakes on the Byers Peninsula (Toro
et al. 2007). During the last 25 years, owing to the environmental changes and the
climate change-driven expansion of permanent ice-free habitats, B. poppei colonised
many newly-formed temporary shallow water bodies in the north-west part of the
Hurd Peninsula (Evtimova et al. 2021).

Boeckella poppei is known to have a wide plasticity to the specific polar environ-
mental conditions, a result of various adaptations, including carotenoid pigmentation
(Byron 1982) and photoprotection through the use of “sunscreen” compounds, for ex-
ample, mycosporine-like amino acids (Rocco et al. 2002). Nevertheless, the population
of B. poppei from Livingston Island demonstrates relatively high morphological vari-
ability and teratology (Pandourski and Chipev 1999; Pandourski and Evtimova 2009).

Here, we describe for the first time a sexually-manifested variation of pigmentation
in B. poppei, inhabiting shallow temporary freshwater ponds on permafrost sediments.

Material and methods

We sampled two adjacent temporary turbid freshwater shallow ponds (with coordi-
nates 62.63622°S, 60.35117°W and an altitude of 23 m a.s.l.) on 07.02.2020. The
ponds were situated on permafrost sediments; dense and thick flocculation of microal-
gae and diatoms covered the ponds’ bottom and edges (Fig. 1). The water transparency
was very low due to colloidal inorganic particles, originating from glacier activity. Their
depths did not exceed 10—12 cm, allowing solar radiation to penetrate to the bottom of
the ponds. The bottom of the ponds was covered with a layer of fine inorganic particles
and cobbles a few cm deep.

Basic physical and chemical characteristics of the water (Tablel1) were measured
using hand-held oximeter Oxi 300i with DurOx 325 electrode and conductometer
Cond 330i with KLE 325 electrode (WTW, Germany).

The specimens of B. poppei were collected with a hand-held net (50 um mesh size)
after intensive mixing of the water. They were transported alive to the laboratory of the

Bulgarian Antarctic Base, immobilised in highly diluted ethanol and photographed.

Sex differenceses in pigmentation of Boeckella poppei from Livingston Island 265

Figure |. General view of pond 1 (a) and flocculation of microalgae and diatoms in pond 2 (b). Photo:
I. Pandourski.

Table |. Basic characteristics of the two ponds.

Pond Area Water temperature Salinity Oxygen Conductivity
(m?) CC) (%o) (mg.dm*) (%) (uS.cm')
10-12 7.6 0.00 8.4 74 82

2 5-6 9.1 0.00 9-5 81 131

Males, copepodites and females (ovigerous and non-ovigerous) were separated, based
on the level of their morphological development and the morphological features typi-
cal for the species following published descriptions of the species (e.g. Bayly 1992).
Body pigmentation was assessed visually in circa 100 individuals (males and females)
from each pond. The basic morphometric characteristics of males and females in a
population from Livingston Island are presented in Pandourski and Chipev (1999).

Results

We observed clearly manifested differences in body pigmentation of ovigerous females
vs. adult males, non-ovigerous females and copepodites of B. poppei. The body of ovi-
gerous females was depigmented, almost transparent, while their egg sacs were from
red to dark orange. Ingested algae with a high concentration of pigments were clearly
visible in their gut content (Fig. 2). Of the studied specimens, all mature females ex-
hibited the described colouration. The body of males and non-ovigerous females was
dark orange or red-coloured due to the even distribution of pigments (Fig. 3).

Discussion

We describe for the first time sexually-manifested pigmentation of B. poppei. Pig-
ments were evenly distributed throughout the body of all specimens, except for ma-
ture ovigerous females, where they were concentrated in the egg sacs. Reddish colour-
ation in copepods is caused by different carotenoids synthesised from the B-carotene

266 Ivan Pandourski et al. / BioRisk 17: 263-269 (2022)

Figure 2. Depigmented, almost transparent body of mature females of Boeckella poppei with intensely
pigmented ovisacs (above) and males with evenly pigmented bodies (below). Photo: L. Kenderov.

a Imm b inant

Figure 3. Boeckella poppei: two evenly pigmented males and one non-ovigerous female (a) and a mature
female with almost transparent body and intensely pigmented ovisacs (b). Photo: L. Kenderov.

present in the algae used as a food source (Ringelberg 1980). One of the functions of
this pigmentation is photoprotection. The synthesis of photoprotective compounds
in the body of copepods is amongst the most important strategies to avoid the dam-
aging effect of UVR in the Antarctic (Rocco et al. 2002) and high- latitude environ-
ments (Hansson 2004), as well as in alpine lakes (Tartarotti et al. 1999; Tartarotti et

Sex differenceses in pigmentation of Boeckella poppei from Livingston Island 267

al. 2017). Sommaruga (2010) established very high carotenoid concentrations (free
astaxanthin) in calanoid copepods from clear fishless Himalayan alpine lakes. The
concentrations of carotenoids in these copepods were inversely related to the lake
depth refuge, while the lowest concentrations were found in copepods from a turbid
glacier-fed lake.

The studied populations of B. poppe from Livingston Island inhabit small shal-
low turbid ponds. There the photoprotective strategy of migration to the deeper water
layers was not possible as the depth of the ponds was only 5—12 cm and, despite the
high turbidity of the water, the calanoids were likely exposed to the action of the UVR.
In shallow ponds and lakes, the carotenoid pigments are known to play an important
photoprotective role. According to Rocco et al. (2002), only the presence of photopro-
tection could be demonstrated in populations of B. poppei from the studied lakes on
the Antarctic Peninsula, while the limited efficiency of enzymatic DNA repair mecha-
nisms could be related to the low temperatures prevailing in Antarctic lakes.

In Antarctica, the life cycle of copepods in temporary ponds is controlled by the
alteration between liquid water and ice and only few species can survive in these harsh
conditions (Pociecha and Dumont 2008). Ovogenesis is one of the most sensitive
stages in their life cycles as the damaging and teratogenic effect of UVR could cause
morphological abnormalities incompatible with the survival of the individual. We con-
sider the concentration of practically the whole amount of the accumulated pigments
(as implied by the intensity of the colouration) into the ovisacs of females of B. poppei
a specific strategy to protect progeny from the damaging UVR in the dynamically
changing Antarctic environmental conditions over the past decades, enhancing the
survival of individuals and expanding the range of this species.

Conclusions

The observed phenomenon of concentrating of carotenoid pigments in eggs of oviger-
ous females demonstrates the plasticity of B. poppei to survive in habitats exposed to
high UVR. Further studies are needed to establish the type of the pigments and the
mechanisms of their accumulation in the ovisacs. We suggest this pigmentation is a
strategy for avoiding the teratogenic effects of UVR and for progeny protection. ‘This,
in turn, is facilitating the expansion of B. poppei in Antarctica through colonisation
and survival in freshwater habitats, newly formed after the retreat of permanent ice
cover. Thus, B. poppei could be a suitable indicator for reflecting the ongoing global
environmental changes in Antarctica.

Acknowledgements

The authors are grateful to the National Center of Polar Research, Bulgarian Antarctic
Institute and the staff of the 28" Bulgarian Antarctic Expedition for their logistic sup-
port and Prof. D.Sc. Ch. Pimpirev and D. Mateev.

268 Ivan Pandourski et al. / BioRisk 17: 263-269 (2022)

This study was funded through the National Program for Polar Studies, Polar Re-
search Funding: projects # 70.25-178/22.11.2019, 70.25-177/22.11.2019 and 70-25-
68/03.08.2021.

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